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R E S E A R C H Open AccessHuman herpesvirus-8 in northwestern China: epidemiology and characterization among blood donors Xing Wang1, Bin He2, Zhaoxia Zhang1, Tao Liu1, Hui Wang1, Xu Li

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R E S E A R C H Open Access

Human herpesvirus-8 in northwestern China:

epidemiology and characterization among blood donors

Xing Wang1, Bin He2, Zhaoxia Zhang1, Tao Liu1, Hui Wang1, Xu Li3, Qiong Zhang1, Ke Lan4, Xiaomei Lu1,

Hao Wen1*

Abstract

Background: Human herpes virus 8 (HHV-8) is the etiologic agent associated with development of classical, AIDS-related, iatrogenic, and endemic Kaposi’s sarcoma (KS) Several studies provide strong evidence that HHV-8 can be transmitted by blood transfusion We evaluated the seroprevalence and potential risk factors of HHV-8 infection in blood donors in one region We surveyed HHV-8 infection among 4461 blood donors in Xinjiang, China, a unique endemic area for HHV-8 and KS

Results: The HHV-8 seroprevalence was higher in local minority groups which comprise most KS cases in China, than in Han people HHV-8 prevalence was 18.6% in the Han ethnic group, 25.9% in Uygur subjects, 29.2% in Kazak subjects, 36.8% in Mongolian subjects, and 21.9% in other ethnic groups In several subgroups, the time of

donation of whole blood seemed to be a risk factor In HHV-8-seropositive subjects, a larger fraction of local

minorities (23.9%) had high HHV-8 titers than that of Han subjects (9.2%) HHV-8 infection was associated with ethnicity and residence

Conclusion: HHV-8 seroprevalence was significantly high among blood donors in Xinjiang, where the prevalence

of KS correlates with HHV-8 prevalence and titers in Uygur and Kazak ethnic groups Blood exposure represented

by the frequency of blood donation indicated a possible blood-borne transmission route of HHV-8 in Xinjiang Detecting anti-HHV-8 antibodies before donation in this region is therefore important

Background

Human herpes virus 8 (HHV-8) is the etiologic agent

associated with the development of classical,

AIDS-related, iatrogenic, and endemic Kaposi’s sarcoma (KS)

[1,2] HHV-8 is also associated with lymphoproliferative

diseases, including primary effusion lymphomas and

multicentric Castleman’s disease [3,4] Emerging

evi-dence suggests that HHV-8 may be transmitted through

sexual contact [5,6], saliva [7], and blood transfusion

[8-10] In the USA, where HHV-8 seroprevalence is low

(<10%), HHV-8 is spread by the sexual route, at least

among homosexual men [5,6] In regions or countries

with high HHV-8 seroprevalence (>25%), HHV-8

infec-tion increases throughout childhood, suggesting that

transmission occurs through saliva or other horizontal routes [11-13] Of note, HHV-8 infection has been observed in patients who received non-leukocyte-reduced blood [8] Infectious viruses or viral DNA have been identified from blood donors in the USA and Africa [14,15] HHV-8 infection has been observed in patients receiving blood transfusions in Uganda, thereby indicating blood-borne transmission of HHV-8 [9,10] HHV-8 seroprevalence among blood donors varies between different regions HHV-8 prevalence ranges from 0.2% in Japan, 0-15% in the USA and the UK, up

to >50% in some African countries [16,17] There is a wide range of variations in HHV-8 infection in South America [18] A few studies focusing on small study populations have been carried out in China In the inland areas of China, HHV-8 seroprevalence in general population was <8% [19,20] In Xinjiang, in the north-west of China, HHV-8 seroprevalence ranged from

* Correspondence: wangxing7610@yahoo.com.cn

1 First Teaching Hospital of Xinjiang Medical University, Urumqi, Xinjiang,

PR China

© 2010 Wang et al; licensee BioMed Central Ltd This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in

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12.5% to 48% depending on different populations

[21-24] The mode of HHV-8 transmission remains

undefined, but the unique pattern of HHV-8 infection

in this geographic region correlated well with an

increased incidence of KS [21,22,24]

Results

Demographic patterns of HHV-8 seroprevalence among

blood donors

A total of 4461 serum samples from blood donors were

analyzed Demographic patterns and blood

donation-associated behavioral characteristics of HHV-8 infection

are shown in Tables 1 and 2, respectively Overall, 3551 subjects were HHV-8-negative (79.6%) whereas 910 par-ticipants were HHV-8-positive (20.4%) In this popula-tion, there was no significant difference in HHV-8 seroprevalence with respect to sex, age, marriage, occu-pation, education, blood type, and times of donation of blood components Xinjiang residents exhibited HHV-8 seroprevalence of 21.3%, whereas the value for non-resi-dents was 17.7% The latter were all of Han extraction who had migrated to Xinjiang from inland areas There was a difference among ethnic groups HHV-8 seropre-valence in the Han population was lower (18.6%) than

Table 1 Sociodemographic characteristics by HHV-8 seroprevalence

Characteristics Number of subjects (%) HHV-8 sero-positivity (%) OR (95% CI) p

Male 2662 (59.7) 533 (20.0)

Female 1799 (40.3) 377 (21.0)

Han 3386 (75.9) 629 (18.6)

Uygur 526 (11.8) 136 (25.9) 1.5 (1.2-1.9) 0.000* Kazak 161 (3.6) 47 (29.2) 1.8 (1.3-2.6) 0.001* Mongolian 87 (2.0) 32 (36.8) 1.0 (1.6-4.0) 0.000* Other 301 (6.7) 66 (21.9) 2.6 (0.9-1.6) 0.155

19-24 2076 (46.5) 430 (20.7)

24-29 904 (20.3) 166 (18.4) 0.9 (0.7-1.1) 0.141 29-34 590 (13.2) 120 (20.3) 1.0 (0.8-1.2) 0.843 34-39 489 (11.0) 102 (20.9) 1.0 (0.8-1.3) 0.843 39-44 245 (5.5) 56 (22.9) 1.1 (0.8-1.6) 0.436 44-49 105 (2.4) 24 (22.9) 1.1 (0.7-1.8) 0.598 49-54 43 (1.1) 10 (23.3) 1.2 (0.6-2.4) 0.684

>54 9 (0.2) 2 (22.2) 1.1 (0.2-5.3) 0.911 Martial status 1.1 (0.9-1.3) 0.301 Unmarried 3078 (69.0) 615 (20.0)

Ever married 1383 (31.0) 295 (21.3)

Soldier 157 (3.5) 25 (15.9)

Student 1290 (28.9) 276 (21.4) 1.4 (0.9-2.2) 0.112 Professional specialty 740 (16.6) 159 (21.5) 1.4 (0.9-2.3) 0.118 Business\service 697 (15.6) 125 (17.9) 1.0 (0.7-1.8) 0.550 Unidentified job 1577 (35.4) 325 (20.6) 1.3 (0.9-2.1) 0.165

College 1034 (23.2) 217 (21.0)

Junior College 1080 (24.2) 237 (21.9) 1.0 (0.9-1.3) 0.592 Technical Secondary School 459 (10.3) 79 (17.2) 0.8 (0.6-1.0) 0.092 Senior High School 935 (21.0) 197 (21.1) 1.0 (0.9-1.2) 0.964 Junior High School 844 (18.9) 162 (19.2) 0.9 (0.7-1.1) 0.336 Elementary School 109 (2.4) 18 (16.5) 0.3 (0.3-0.9) 0.273 Residence 1.3 (1.1-1.5) 0.009* Xinjiang 3321 (74.4) 708 (21.3)

Outside of Xinjiang 1140 (25.6) 202 (17.7)

Total 4461 (100.0) 910 (20.4)

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in any other ethnic group, such as Uygur (25.9%), Kazak

(29.2%), Mongolian (36.8%) and others (21.9%) HHV-8

seroprevalence tended to increase among local minority

groups Most individuals were blood donors, who were

negative for hepatitis-B virus (HBV), hepatitis-C virus

(HCV), human immunodeficiency virus (HIV), and

syphilis (99.8%) Among seven positive subjects for these

pathogens, three were HHV-8-positive individuals

(42.9%) The relevance of HBV, HCV, HIV, and syphilis

to HHV-8 seroprevalence was not further analyzed

because the small sample size

Assessment of risk factors

The univariate associations between HHV-8

seroprave-lence and subject characteristics are illustrated in Tables

1 and 2 Ethnic background was found to be associated

with HHV-8-positive status This variable exhibited a

statistically significant difference whereby the odds ratio

(OR) was high for Uygur (1.5, 95% confidence interval

(CI) 1.2-1.9, p < 0.000) and Kazak (1.8, 95% CI 1.3-2.6,

p < 0.001) ethnic groups Residence appeared to be

associated with HHV-8 infection (OR = 1.3, 95% CI

1.1-1.5, p < 0.009) No associations were observed between

HHV-8 seroprevalence and sex, age, education, marital

status, occupation and blood donation-associated

behaviors To further identify independent risk factors, all variables from the univariate analysis were entered into multiple logistic regression models (Table 3) In this analysis, HHV-8-positive status was associated with Uygur (OR = 1.4, 95% CI 1.1-1.9, p < 0.000) and Kazak (OR = 1.8, 95% CI 1.2-2.6, p < 0.000) ethnic groups

Table 2 HHV-8 seroprevalence by blood donor-associated behaviors

Characteristics Number of subjects (%) HHV-8 sero-positivity (%) OR (95% CI) p Type of blood donation 1.0(0.7-1.4) 0.962 Whole blood 4232 (94.9) 863 (20.4)

Blood component 229 (5.1) 47 (20.5)

Time of donation of whole blood 0.845

1 2702(63.8) 557 (20.6)

2 851 (20.1) 176 (20.7) 1.0 (0.7-1.4) 0.958

3 352 (8.3) 76 (21.6) 0.0 (0.7-1.4) 0.758

4 168 (4.0) 25 (14.9) 1.1 (0.7-1.6) 0.151

5 67 (1.6) 13 (19.4) 0.7 (0.4-1.2) 0.841

6 39 (0.9) 7 (17.9) 0.9 (0.5-1.9) 0.711

7 25 (0.6) 4 (16.0) 0.8 (0.4-2.0) 0.593

8 28 (0.7) 5 (17.9) 0.7 (0.2-2.3) 0.740 Time of donation of blood components 0.678 1-5 64 (27.9) 13 (20.3)

6-10 29 (12.7) 10 (34.5) 1.0 (0.5-1.8) 0.067 12-15 33 (14.4) 6 (18.2) 2.1 (1.0-4.4) 0.987 16-20 24 (10.5) 4 (16.7) 0.9 (0.4-2.1) 0.754 21-25 19 (8.3) 2 (10.5) 0.8 (0.3-2.3) 0.652 26-30 26 (11.4) 5 (19.2) 0.5 (0.1-2.0) 0.299 31-40 20 (8.7) 3 (15.0) 0.9 (0.7-2.5) 0.884 41-44 14 (6.1) 4 (28.6) 0.7 (0.2-2.4) 0.553 Pathogens screen 0.0 (0.0-1.0) 0.982 Seronegative 4452 (99.8) 907 (20.4) 2.9(0.7-13.1) 0.159 Seropositive 7 (0.2) 3 (42.9)

(HBV/HCV/HIV/syphilis)

Table 3 Analyses by risk factor

OR (95% CI) p Ethnic background 0.000*

Uygur 1.4 (1.1-1.9) 0.004* Kazak 1.8 (1.2-2.6) 0.004* Mongolian 2.7 (1.7-4.2) 0.000* Other 1.3 (0.9-1.7) 0.142 Time of donation of whole blood 0.185

2 1.2 (0.9-1.7) 0.291

3 1.9 (1.1-3.2) 0.021*

4 1.5 (0.7-3.0) 0.278

5 3.5 (1.3-9.7) 0.016*

6 4.6 (1.2-17.8) 0.025*

7 4.1 (0.8-20.7) 0.089

8 5.1 (1.1-23.9) 0.040*

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A strong association of HHV-8 infection was seen with

the Mongolian (OR = 2.7, 95% CI 1.7-4.2, p < 0.000)

ethnic group With the increasing frequency of donation

of whole blood, the possibility of infection also increased

in several subgroups such as 3 (OR = 1.9, 95% CI

1.1-3.2, p < 0.021), 5 (OR = 3.5, 95% CI 1.3-9.7, p < 0.016),

6 (OR = 4.6, 95% CI 1.2-17.8, p < 0.025), and 8 (OR =

5.1, 95% CI 1.1-23.9, p < 0.04) There was no association

between HHV-8 seroprevalence and the other variables

evaluated in Tables 1 and 2 (data not shown)

HHV-8 antibody titers in HHV-8-positive individuals

We compared relative levels of HHV-8 antibody titers

among HHV-8-positive subjects High titers were noted

in: 12.2% of those aged <30 years, 13.4% of subjects

aged >30 years, 12% of unmarried individuals, and

13.9% of married individuals (Figure 1) There was no

major difference in these subgroups Among study

sub-jects, 11.9% of individuals who had a Junior High

School-education had high titers This number increased

to 15.6% for those who studied beyond Junior High

School Only 9.2% of HHV-8-positive subjects from the

Han ethnic group had high titers This number

increased to 23.9% in minority groups which included

the Uygur and Kazak ethnic groups As compared with

subjects from the Han ethnic group, local minorities

had a larger proportion of individuals with a higher

level of HHV-8 antibody titers

We further examined HHV-8 antibody titers in each

individual ethnic group The Han group exhibited a

8 seroprevalence of 18.6%, but only 9.2% of

HHV-8-positive subjects had high anti-HHV-8 titers (Figure

2) A similar trend was seen in the Mongolian group

and other groups except the Uygur and Kazak groups

The Mongolian group showed a HHV-8 seroprevalence

of 36.8%, whereas 18.8% had high HHV-8 antibody titers Other groups showed a HHV-8 seroprevalence of 21.9%, whereas 12.1% had high HHV-8 titers Strikingly, different results were seen in Uygur and Kazak groups; 24.3% of the Uygur group with HHV-8 infection had high 8 titers, and 23.4% of Kazak who were

HHV-8 positive had high HHV-HHV-8 titers Therefore, a larger fraction of Uygur and Kazak groups had higher HHV-8 antibody titers than those in the other ethnic groups

Discussion

The present study was the first large-scale survey of HHV-8 seroprevalence in blood donors in China Recent reports showed that HHV-8 seroprevalence was 7.3% in Liaonin province and 5.7% in Shandong province among healthy blood donors [19,25] These studies focused on the Han ethnic group, and the study population was small A study in the Han ethnic group in Hubei pro-vince revealed that HHV-8 seroprevalence was 5.2% [20] The prevalence of HHV-8 infection reported in these studies was similar to those among the adult population in North America [6,14,26] These observa-tions suggest that HHV-8 seroprevalence in China was,

in general, low The Xinjiang area, located in the north-west of China, exhibited a distinct pattern We noted that HHV-8 seroprevalence was relatively high in the Han ethnic group living in Xinjiang: 18.6% of blood donors were HHV-8 positive Moreover, HHV-8 sero-prevalence was 17.7% among the 1140 non-residential Han ethnic group who migrated to Xinjiang from inland areas Thus, an elevated HHV-8 seroprevalence in the Han ethnic group in Xinjiang province implies an asso-ciation of HHV-8 infection with the living environment These potential factors which contribute to the differ-ences within the same ethnic group suggest an increased

Figure 1 Relative HHV-8 high titers in different subgroups among blood donors.

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opportunity for members of the Han ethnic group to

have close contact with highly infected populations And

the relatively low level of public health in Xinjiang

pro-vince due to the economic situation in this region may

benefit the spread or transmission of HHV-8, but this

hypothesis needs conformation The precise impact of

being resident in Xinjiang on HHV-8 infection could

not be ascertained because of the cross-sectional nature

of the present study

The present study suggested that HHV-8

seropreva-lence was associated with ethnicity but not with sex,

age, marital status, occupation, educational level, blood

type, and time of donation of blood components

Among blood donors, HHV-8 seroprevalence was 18.6%

in the Han group, 25.9% in the Uygur group, 29.2% in

the Kazak group, and 36.8% in the Mongolian group

When combined, the mean prevalence of HHV-8

infec-tion in local minorities was 30.6% Compared with Han

subjects living in Xinjiang, the elevated HHV-8

seropre-valence in local minorities was significant Hence, what

was the basis for the observed differences? It is known

that local minorities have resided in Xinjiang for

genera-tions, and that they have unique cultural practices An

intriguing possibility is that different cultural practices

or social behaviors may play a part in HHV-8 infection

Alternatively, genetic factors may affect the susceptibility

to HHV-8 infection Additional studies are required to

address these issues

Several studies have demonstrated that HHV-8

sero-prevalence is correlated with the occurrence of KS in

Europe and Africa [27-30] In Ghana and Egypt, a high

prevalence of HHV-8 does not correlate well with KS

onset [11,31] HHV-8 seroprevalence is high among

Amerindians in Brazil, French Guiana and Ecuador [32-34] Nonetheless, KS has not been reported for these populations The present study revealed that HHV-8 seroprevalence was higher in Han subjects resid-ing in Xinjiang than in the inland areas of China Furthermore, it was higher in local minority groups than in Han subjects HHV-8 prevalence remained high

in blood donors residing in Xinjiang, but classical KS and AIDS-related KS were observed only among local minority groups [21,22] Taken together, these data sup-port the hypothesis that additional factors other than HHV-8 may be involved in KS development

Several researchers reported blood-borne transmission

of HHV-8 among a large cohort of drug users, or pro-spective studies on blood-transfusion recipients [8,10] The present study was in accordance with these studies because it established a positive relationship between an increasing prevalence of infection with the correspond-ing frequency of donation of whole blood To a certain extent, the time of donation represents the opportunity

of blood exposure In China, laws pertaining to donation

of whole blood were passed in 1992 Before 1992, non-standard protocols for blood collection, and absence of instruments and materials were common These condi-tions could increase the prevalence of HHV-8 infection

by blood exposure A possible explanation for the con-tradictory results in the univariate analysis with respect

to the time of donation of blood components may be due to the small number of samples in each group or undetermined factors

There was a difference in HHV-8 antibody titers among HHV-8-seropositive individuals in the present study Specifically, a larger fraction of local minorities

Figure 2 HHV-8 infection by seroprevalence and high antibody titers in different ethnic groups

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had high HHV-8 antibody titers than Han subjects This

was evident in the Uygur and Kazak ethnic groups

Whether this reflects enhanced replication of HHV-8 or

enhanced immune responses is not clear Notably, KS

patients are seen in Uygur and Kazak ethnic groups in

Xinjiang hospitals [21,22] The patients are typically

elderly men who have multiple nodular lesions in the

lower or upper extremities Intriguingly, KS patients

tend to be younger among those who are also infected

with HIV Hence, high HHV-8 antibody titers in Uygur

and Kazak groups appeared to correlate with the

devel-opment of KS in these ethnic groups

Conclusions

HHV-8 seroprevalence was significantly high in blood

donors from Xinjiang A critical question relevant to

public health is if HHV-8 is transmitted through blood

transfusion in the Xinjiang area Several studies in the

USA and Africa suggest an association between HH-8

infection with blood transfusion Error! Reference source

not found Given that HHV-8 seroprevalence in the

Xin-jiang area is high, assessing the risk of HHV-8

transmis-sion via blood transfutransmis-sion in future studies is essential

Methods

Ethical approval of the study protocol

The present study was approved by the Institutional

Ethics Committee of the First Teaching Hospital of

Xin-jiang Medical University (Urumqi, XinXin-jiang, China)

Written informed consent was obtained from all

sub-jects, and patient confidentiality was ensured

Study population

A cross-sectional study was designed to assess the

sero-prevalence of HHV-8 infection among blood donors in

Xinjiang, China Serum samples, collected and deposited

from all five blood banks belonging to Xinjiang Blood

Center between August 2006 and May 2007, were

ana-lyzed These samples were derived from 4832 blood

donors belonging to different ethnic groups: Han,

Uygur, Kazak, Mongolian, and others All samples went

through a standard screening for HBV, HCV, HIV, and

syphilis A questionnaire regarding age, sex, ethnicity,

marital status, education and residence was collected Of

4832 blood donors, 4461 blood donors completed all

sections of the questionnaire Serum samples were

cen-trifuged and stored at -80°C before HHV-8 serologic

testing

Laboratory procedures

The coded serum specimens were tested for HHV-8

anti-gens of ORF73, ORF65and K8.1 using enzyme-linked

immunosorbent assays as described22,24Error! Reference

source not found This assay has a sensitivity of 82% and

a specificity of 96%22 Briefly, viral antigen-coated plates were incubated with serum samples diluted at 1:100 This was followed by incubation with goat anti-human immu-noglobulins (including IgG) conjugated with horseradish peroxidase (HRP; Tago Immunologicals) The mean opti-cal density at 450 nm was determined Controls included serum samples derived from KS patients and HHV-8-negative individuals Based on the assays from control groups, the HHV-8-positive cutoff was set to the value that was three-times that of the negative control The HHV-8 high titer was set to the value that was more than five-times that of the negative control

Statistical analyses

All statistical analyses were carried out using SPSS soft-ware version 12.0 (SPSS Incorporated, Chicago, IL, USA) The univariate analysis of categorical variables was evalu-ated by #2 test withP < 0.05 being considered significant Associations revealed by OR and P were evaluated at a

CI of 95% Multivariate logistic regression analysis was carried out to control for confounding factors CI was calculated based on coefficients and standard errors from the logistic model Seropositive prevalence and risk fac-tors were compared between groups

Acknowledgements This work was supported by the Youth Funds of Xinjiang Autonomous Region (grant number 2009211B17) and the Joint Funds of the National Natural Science Foundation of China (30760228).

Author details

1 First Teaching Hospital of Xinjiang Medical University, Urumqi, Xinjiang,

PR China.2Department of Microbiology and Immunology, College of Medicine, the University of Illinois at Chicago, IL 60612, USA 3 Blood Center

of Urumqi, Xinjiang, PR China.4Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai, PR China.

Authors ’ contributions

XW carried out study design, sample collection, and statistical analyses performance; she also participated in antibody detection ZZ, TL, QZ and HW also participated in antibody detection XLi and XLu wrote and collected the questionnaire BH drafted the manuscript KL participated in the design of the study and carried out statistical analyses.

HW conceived the study, and participated in its design and coordination; he also helped to draft the manuscript All authors read and approved the final manuscript.

Competing interests The authors declare that they have no competing interests.

Received: 29 November 2009 Accepted: 17 March 2010 Published: 17 March 2010

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doi:10.1186/1743-422X-7-62 Cite this article as: Wang et al.: Human herpesvirus-8 in northwestern China: epidemiology and characterization among blood donors Virology Journal 2010 7:62.

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